Dissecting the black box of microbially mediated pyrite formation from FeS and H2S

• Applicant: Professor Dr. Michael Pester
• Subject Area: Metabolism, Biochemistry and Genetics of Microorganisms ; Microbial Ecology and Applied Microbiology
• Term: from 2019 to 2024
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 435849387

• Final Report Year: 2024

Final Report Abstract

Pyrite has been formed in large quantities in sediments since the Archean, which not only had a major impact on the global sulfur and iron cycle, but also on the redox state of the atmosphere. The mechanisms behind sedimentary pyrite formation and the influence of microorganisms on it are still unclear. In 2019, we were able to describe the first microbial enrichment culture (J5) that can form FeS2 and CH4 from FeS, H2S, and CO2 as sole substrates (Thiel et al., 2019, PNAS). This proposal aimed to elucidate the mechanisms of pyrite formation in enrichment J5. The start of the project overlapped with the beginning of the corona crisis, which led to personnel difficulties in the further course of the project. At the same time, there was a shortage of commercially available, high-purity Na2S crystals, which J5 requires as a starting substrate for H2S. This shortage is ongoing until today. These circumstances forced us to perform a reorientation of the project. In the first phase of the reorientation, we concentrated on the isolation and characterization of the individual bacterial and archaeal species from the J5 enrichment. This resulted in the characterization of a new methanogenic archaeal species and a new sulfur-reducing bacterial species within the project, as well as a new sulfate-reducing bacterial species outside the project. In parallel, an attempt was made to produce high-purity Na2S in the laboratory, but this was not successful. Due to the long generation times of the J5 culture (approx. 6 months), it could only be adapted very slowly to commercially available Na2S, but this was achieved at the end of the project. In the meantime, we concentrated on analyzing novel microorganisms and their physiologies in the sulfur cycle. In an article in FEMS Microbiology Reviews, we revealed that 19 of 23 bacterial and 2 of 4 archaeal phyla contained previously unknown sulfate reducers. A subsequent publication in Nature Communications showed that representatives of the Acidobacteriota can switch between sulfate respiration and oxygen respiration - a novelty in the sulfur cycle. Within the same experiment, already known groups of sulfate reducers were also able to build up large populations, despite long and recurring exposure to an O2-containing atmosphere. A subsequent article (accepted for publication in Microbiome) was able to show the multiple strategies of oxygen detoxification within these microorganisms. As a by-product of these activities, a new Desulfosporosinus species was described (submitted to IJSEM).

Publications

• Aminithiophilus ramosus gen. nov., sp. nov., a sulphur-reducing bacterium isolated from a pyrite-forming enrichment culture, and taxonomic revision of the family Synergistaceae. International Journal of Systematic and Evolutionary Microbiology, 73(2).
  Pradel, Nathalie; Fardeau, Marie-Laure; Bunk, Boyke; Spröer, Cathrin; Boedeker, Christian; Wolf, Jacqueline; Neumann-Schaal, Meina; Pester, Michael & Spring, Stefan
  
• Global diversity and inferred ecophysiology of microorganisms with the potential for dissimilatory sulfate/sulfite reduction. FEMS Microbiology Reviews, 47(5).
  Diao, Muhe; Dyksma, Stefan; Koeksoy, Elif; Ngugi, David Kamanda; Anantharaman, Karthik; Loy, Alexander & Pester, Michael
  
• Oxygen respiration and polysaccharide degradation by a sulfate-reducing acidobacterium. Nature Communications, 14(1).
  Dyksma, Stefan & Pester, Michael
  
• Description and genome analysis of a novel archaeon isolated from a syntrophic pyrite-forming enrichment culture and reclassification of Methanospirillum hungatei strains GP1 and SK as Methanospirillum purgamenti sp. nov.. PLOS ONE, 19(8), e0308405.
  Pradel, Nathalie; Bartoli, Manon; Koenen, Michel; Bale, Nicole; Neumann-Schaal, Meina; Spröer, Cathrin; Bunk, Boyke; Rohde, Manfred; Pester, Michael & Spring, Stefan
  
• Growth of sulfate-reducing Desulfobacterota and Bacillota at periodic oxygen stress of 50% air-O2 saturation. Microbiome, 12(1).
  Dyksma, Stefan & Pester, Michael